1887

Abstract

The climate-active gas isoprene is the major volatile produced by a variety of trees and is released into the atmosphere in enormous quantities, on a par with global emissions of methane. While isoprene production in plants and its effect on atmospheric chemistry have received considerable attention, research into the biological isoprene sink has been neglected until recently. Here, we review current knowledge on the sources and sinks of isoprene and outline its environmental effects. Focusing on degradation by microbes, many of which are able to use isoprene as the sole source of carbon and energy, we review recent studies characterizing novel isoprene degraders isolated from soils, marine sediments and in association with plants. We describe the development and use of molecular methods to identify, quantify and genetically characterize isoprene-degrading strains in environmental samples. Finally, this review identifies research imperatives for the further study of the environmental impact, ecology, regulation and biochemistry of this interesting group of microbes.

Funding
This study was supported by the:
  • J. Colin Murrell , H2020 European Research Council , (Award IsoMet 694578)
  • J. Colin Murrell , Natural Environment Research Council , (Award NE/J009725/1)
  • Terry J McGenity , Natural Environment Research Council , (Award NE/J009555/1)
  • Andrew Crombie , Leverhulme Trust , (Award ECF-2016-626)
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000931
2020-05-22
2020-06-02
Loading full text...

Full text loading...

/deliver/fulltext/micro/10.1099/mic.0.000931/mic000931.html?itemId=/content/journal/micro/10.1099/mic.0.000931&mimeType=html&fmt=ahah

References

  1. Guenther A, Karl T, Harley P, Wiedinmyer C, Palmer PI et al. Estimates of global terrestrial isoprene emissions using MEGAN (model of emissions of gases and aerosols from nature). Atmos Chem Phys 2006; 6:3181–3210 [CrossRef]
    [Google Scholar]
  2. Guenther AB, Jiang X, Heald CL, Sakulyanontvittaya T, Duhl T et al. The model of emissions of gases and aerosols from nature version 2.1 (MEGAN2.1): an extended and updated framework for modeling biogenic emissions. Geosci Model Dev 2012; 5:1471–1492 [CrossRef]
    [Google Scholar]
  3. Royal Society Ground-level Ozone in the 21st Century: Future Trends, Impacts and Policy Implications. Science Policy Report 15/08 London: The Royal Society; 2008
    [Google Scholar]
  4. Carlton AG, Wiedinmyer C, Kroll JH. A review of secondary organic aerosol (SOA) formation from isoprene. Atmos. Chem. Phys. 2009; 9:4987–5005 [CrossRef]
    [Google Scholar]
  5. Pacifico F, Harrison SP, Jones CD, Sitch S. Isoprene emissions and climate. Atmos Environ 2009; 43:6121–6135 [CrossRef]
    [Google Scholar]
  6. Rohmer M. The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat Prod Rep 1999; 16:565–574 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  7. Sharkey TD, Wiberley AE, Donohue AR. Isoprene emission from plants: why and how. Ann Bot 2008; 101:5–18 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  8. Loreto F, Ciccioli P, Brancaleoni E, Valentini R, De Lillis M et al. A hypothesis on the evolution of isoprenoid emission by oaks based on the correlation between emission type and Quercus taxonomy. Oecologia 1998; 115:302–305 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  9. Sharkey TD, Yeh S. Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol 2001; 52:407–436 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  10. Zeinali N, Altarawneh M, Li D, Al-Nu'airat J, Dlugogorski BZ. New mechanistic insights: why do plants produce isoprene?. ACS Omega 2016; 1:220–225 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  11. Magel E, Mayrhofer S, Müller A, Zimmer I, Hampp R et al. Photosynthesis and substrate supply for isoprene biosynthesis in poplar leaves. Atmos Environ 2006; 40:138–151 [CrossRef]
    [Google Scholar]
  12. Loivamäki M, Mumm R, Dicke M, Schnitzler J-P. Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proc Natl Acad Sci U S A 2008; 105:17430–17435 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  13. Zuo Z, Weraduwage SM, Lantz AT, Sanchez LM, Weise SE et al. Isoprene acts as a signaling molecule in gene networks important for stress responses and plant growth. Plant Physiol 2019; 180:124–152 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  14. Lantz AT, Allman J, Weraduwage SM, Sharkey TD. Isoprene: new insights into the control of emission and mediation of stress tolerance by gene expression. Plant Cell Environ 2019; 42:2808–2826 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  15. Sharkey TD, Monson RK. Isoprene research - 60 years later, the biology is still enigmatic. Plant Cell Environ 2017; 40:1671–1678 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  16. Ashworth K, Wild O, Hewitt CN. Impacts of biofuel cultivation on mortality and crop yields. Nat Clim Chang 2013; 3:492–496 [CrossRef]
    [Google Scholar]
  17. Hewitt CN, MacKenzie AR, Di Carlo P, Di Marco CF, Dorsey JR et al. Nitrogen management is essential to prevent tropical oil palm plantations from causing ground-level ozone pollution. Proc Natl Acad Sci U S A 2009; 106:18447–18451 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  18. Monson RK, Winkler B, Rosenstiel TN, Block K, Merl-Pham J et al. High productivity in hybrid-poplar plantations without isoprene emission to the atmosphere. Proc Natl Acad Sci U S A 2020; 117:1596–1605 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  19. Gelmont D, Stein RA, Mead JF. Isoprene-the main hydrocarbon in human breath. Biochem Biophys Res Commun 1981; 99:1456–1460 [CrossRef]
    [Google Scholar]
  20. Fall R, Copley SD. Bacterial sources and sinks of isoprene, a reactive atmospheric hydrocarbon. Environ Microbiol 2000; 2:123–130 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  21. Exton DA, McGenity TJ, Steinke M, Smith DJ, Suggett DJ. Uncovering the volatile nature of tropical coastal marine ecosystems in a changing world. Glob Chang Biol 2015; 21:1383–1394 [CrossRef]
    [Google Scholar]
  22. Deneris ES, Stein RA, Mead JF. Invitro biosynthesis of isoprene from mevalonate utilizing a rat liver cytosolic fraction. Biochem Biophys Res Commun 1984; 123:691–696 [CrossRef]
    [Google Scholar]
  23. Stönner C, Williams J. Goals change crowd air chemistry. Nature 2016; 535:355 [CrossRef]
    [Google Scholar]
  24. Kuzma J, Nemecek-Marshall M, Pollock WH, Fall R. Bacteria produce the volatile hydrocarbon isoprene. Curr Microbiol 1995; 30:97–103 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  25. Shaw SL, Gantt B, Meskhidze N. Production and emissions of marine isoprene and monoterpenes: a review. Advances in Meteorology 2010; 2010:1–24 [CrossRef]
    [Google Scholar]
  26. McGenity TJ, Crombie AT, Murrell JC. Microbial cycling of isoprene, the most abundantly produced biological volatile organic compound on earth. Isme J 2018; 12:931–941 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  27. Exton DA, Suggett DJ, Steinke M, McGenity TJ. Spatial and temporal variability of biogenic isoprene emissions from a temperate estuary. Global Biogeochem Cycles 2012; 26:GB2012 [CrossRef]
    [Google Scholar]
  28. Hackenberg SC, Andrews SJ, Airs R, Arnold SR, Bouman HA et al. Potential controls of isoprene in the surface Ocean. Global Biogeochem Cycles 2017; 31:644–662 [CrossRef]
    [Google Scholar]
  29. Meskhidze N, Sabolis A, Reed R, Kamykowski D. Quantifying environmental stress-induced emissions of algal isoprene and monoterpenes using laboratory measurements. Biogeosciences 2015; 12:637–651 [CrossRef]
    [Google Scholar]
  30. ACIA Impacts of a Warming Arctic: Arctic Climate Impact Assessment. ACIA Overview Report Cambridge, UK: Cambridge University Press; 2004
    [Google Scholar]
  31. Potosnak MJ, Baker BM, LeStourgeon L, Disher SM, Griffin KL et al. Isoprene emissions from a tundra ecosystem. Biogeosciences 2013; 10:871–889 [CrossRef]
    [Google Scholar]
  32. Haapanala S, Rinne J, Pystynen K-H, Hellén H, Hakola H et al. Measurements of hydrocarbon emissions from a boreal fen using the REA technique. Biogeosciences 2006; 3:103–112 [CrossRef]
    [Google Scholar]
  33. Tiiva P, Rinnan R, Faubert P, Räsänen J, Holopainen T et al. Isoprene emission from a subarctic peatland under enhanced UV-B radiation. New Phytol 2007; 176:346–355 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  34. Janson R, De Serves C, Romero R. Emission of isoprene and carbonyl compounds from a boreal forest and wetland in Sweden. Agricultural and Forest Meteorology 1999; 98-99:671–681 [CrossRef]
    [Google Scholar]
  35. Ekberg A, Arneth A, Hakola H, Hayward S, Holst T. Isoprene emission from wetland sedges. Biogeosciences 2009; 6:601–613 [CrossRef]
    [Google Scholar]
  36. Lindwall F, Svendsen SS, Nielsen CS, Michelsen A, Rinnan R. Warming increases isoprene emissions from an Arctic fen. Sci Total Environ 2016; 553:297–304 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  37. Rinnan R, Steinke M, McGenity T, Loreto F. Plant volatiles in extreme terrestrial and marine environments. Plant Cell Environ 2014; 37:1776–1789 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  38. Steinke M, Hodapp B, Subhan R, Bell TG, Martin-Creuzburg D. Flux of the biogenic volatiles isoprene and dimethyl sulfide from an oligotrophic lake. Sci Rep 2018; 8:630 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  39. Borbon A, Fontaine H, Veillerot M, Locoge N, Galloo JC et al. An investigation into the traffic-related fraction of isoprene at an urban location. Atmos Environ 2001; 35:3749–3760 [CrossRef]
    [Google Scholar]
  40. Khan M, Schlich B-L, Jenkin M, Shallcross B, Moseley K et al. A two-decade anthropogenic and biogenic isoprene emissions study in a London urban background and a London urban traffic site. Atmosphere 2018; 9:387 [CrossRef]
    [Google Scholar]
  41. Sahu LK, Yadav R, Pal D. Source identification of VOCs at an urban site of Western India: effect of marathon events and anthropogenic emissions. J Geophys Res 2016; 121:2416–2433 [CrossRef]
    [Google Scholar]
  42. Köksal M, Zimmer I, Schnitzler J-P, Christianson DW. Structure of isoprene synthase illuminates the chemical mechanism of teragram atmospheric carbon emission. J Mol Biol 2010; 402:363–373 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  43. Sivy TL, Shirk MC, Fall R. Isoprene synthase activity parallels fluctuations of isoprene release during growth of Bacillus subtilis. Biochem Biophys Res Commun 2002; 294:71–75 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  44. Ye L, Lv X, Yu H. Engineering microbes for isoprene production. Metab Eng 2016; 38:125–138 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  45. Cleveland CC, Yavitt JB. Consumption of atmospheric isoprene in soil. Geophys Res Lett 1997; 24:2379–2382 [CrossRef]
    [Google Scholar]
  46. Cleveland CC, Yavitt JB. Microbial consumption of atmospheric isoprene in a temperate forest soil. Appl Environ Microbiol 1998; 64:172–177 [CrossRef]
    [Google Scholar]
  47. Pegoraro E, Abrell L, Van Haren J, Barron-Gafford G, Grieve KA et al. The effect of elevated atmospheric CO2 and drought on sources and sinks of isoprene in a temperate and tropical rainforest mesocosm. Glob Chang Biol 2005; 11:1234–1246 [CrossRef]
    [Google Scholar]
  48. Pegoraro E, REY ANA, Abrell L, Haren J, Lin G. Drought effect on isoprene production and consumption in biosphere 2 tropical rainforest. Glob Chang Biol 2006; 12:456–469 [CrossRef]
    [Google Scholar]
  49. Gray CM, Helmig D, Fierer N. Bacteria and fungi associated with isoprene consumption in soil. Elem. Sci. Anth. 2015; 3:000053 [CrossRef]
    [Google Scholar]
  50. Crombie AT, Larke-Mejia NL, Emery H, Dawson R, Pratscher J et al. Poplar phyllosphere harbors disparate isoprene-degrading bacteria. Proc Natl Acad Sci U S A 2018; 115:13081–13086 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  51. Larke-Mejía NL. Molecular Ecology of Isoprene Degraders in the Terrestrial Environment PhD Thesis: University of East Anglia; 2018
    [Google Scholar]
  52. Larke-Mejía NL, Crombie AT, Pratscher J, McGenity TJ, Murrell JC. Novel isoprene-degrading Proteobacteria from soil and leaves identified by cultivation and metagenomics analysis of stable isotope probing experiments. Front Microbiol 2019; 10:2700 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  53. Murphy G. Isoprene Degradation in the Terrestrial Environment PhD Thesis: University of Essex; 2017
    [Google Scholar]
  54. Singh A, Srivastava N, Dubey SK. Molecular characterization and kinetics of isoprene degrading bacteria. Bioresour Technol 2019; 278:51–56 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  55. Acuña Alvarez LA, Exton DA, Timmis KN, Suggett DJ, McGenity TJ. Characterization of marine isoprene-degrading communities. Environ Microbiol 2009; 11:3280–3291 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  56. Booge D, Schlundt C, Bracher A, Endres S, Zäncker B et al. Marine isoprene production and consumption in the mixed layer of the surface ocean – a field study over two oceanic regions. Biogeosciences 2018; 15:649–667 [CrossRef]
    [Google Scholar]
  57. Palmer PI, Shaw SL. Quantifying global marine isoprene fluxes using MODIS chlorophyll observations. Geophys Res Lett 2005; 32:L09805 [CrossRef]
    [Google Scholar]
  58. van Ginkel C, de Jong E, Tilanus JWR, de Bont JAM. Microbial oxidation of isoprene, a biogenic foliage volatile and of 1,3-butadiene, an anthropogenic gas. FEMS Microbiol Lett 1987; 45:275–279 [CrossRef]
    [Google Scholar]
  59. van Ginkel CG, Welten HG, de Bont JA. Oxidation of gaseous and volatile hydrocarbons by selected alkene-utilizing bacteria. Appl Environ Microbiol 1987; 53:2903–2907 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  60. Ewers J, Freier-Schröder D, Knackmuss HJ. Selection of trichloroethene (TCE) degrading bacteria that resist inactivation by TCE. Arch Microbiol 1990; 154:410–413 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  61. Johnston A, Crombie AT, El Khawand M, Sims L, Whited GM et al. Identification and characterisation of isoprene-degrading bacteria in an estuarine environment. Environ Microbiol 2017; 19:3526–3537 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  62. Srivastva N, Shukla AK, Singh RS, Upadhyay SN, Dubey SK. Characterization of bacterial isolates from rubber dump site and their use in biodegradation of isoprene in batch and continuous bioreactors. Bioresour Technol 2015; 188:84–91 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  63. Srivastva N, Vishwakarma P, Bhardwaj Y, Singh A, Manjunath K et al. Kinetic and molecular analyses reveal isoprene degradation potential of Methylobacterium sp. Bioresour Technol 2017; 242:87–91 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  64. Kronen M, Lee M, Jones ZL, Manefield MJ. Reductive metabolism of the important atmospheric gas isoprene by homoacetogens. Isme J 2019; 13:1168–1182 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  65. van Hylckama Vlieg JE, Kingma J, van den Wijngaard AJ, Janssen DB. A glutathione S-transferase with activity towards cis-1, 2-dichloroepoxyethane is involved in isoprene utilization by Rhodococcus sp. strain AD45. Appl Environ Microbiol 1998; 64:2800–2805 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  66. van Hylckama Vlieg JE, Kingma J, Kruizinga W, Janssen DB. Purification of a glutathione S-transferase and a glutathione conjugate-specific dehydrogenase involved in isoprene metabolism in Rhodococcus sp. strain AD45. J Bacteriol 1999; 181:2094–2101 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  67. van Hylckama Vlieg JE, Leemhuis H, Spelberg JH, Janssen DB. Characterization of the gene cluster involved in isoprene metabolism in Rhodococcus sp. strain AD45. J Bacteriol 2000; 182:1956–1963 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  68. Crombie AT, Khawand ME, Rhodius VA, Fengler KA, Miller MC et al. Regulation of plasmid-encoded isoprene metabolism in Rhodococcus, a representative of an important link in the global isoprene cycle. Environ Microbiol 2015; 17:3314–3329 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  69. Leahy JG, Batchelor PJ, Morcomb SM. Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 2003; 27:449–479 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  70. Lienkamp AC, Heine T, Tischler D. Glutathione: a powerful but rare cofactor among actinobacteria. Adv Appl Microbiol 2019In Press
    [Google Scholar]
  71. Dumont MG, Murrell JC. Community-Level analysis: key genes of aerobic methane oxidation. Methods Enzymol 2005; 397:413–427 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  72. El Khawand M, Crombie AT, Johnston A, Vavlline DV, McAuliffe JC et al. Isolation of isoprene degrading bacteria from soils, development of isoA gene probes and identification of the active isoprene-degrading soil community using DNA-stable isotope probing. Environ Microbiol 2016; 18:2743–2753 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  73. Carrión O, Larke-Mejía NL, Gibson L, Farhan Ul Haque M, Ramiro-García J et al. Gene probing reveals the widespread distribution, diversity and abundance of isoprene-degrading bacteria in the environment. Microbiome 2018; 6:219 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  74. Dumont MG, Murrell JC. Stable isotope probing - linking microbial identity to function. Nat Rev Microbiol 2005; 3:499–504 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  75. Dumont MG, Hernández García M. Stable Isotope Probing; Methods and Protocols Totowa, NJ, US: Humana Press; 2019
    [Google Scholar]
  76. Dawson RA, Larke-Mejía NL, Crombie AT, Ul Haque MF, Murrell JC. Isoprene oxidation by the Gram-negative model bacterium Variovorax sp. WS11. Microorganisms 2020; 8:349 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  77. Bender M, Conrad R. Kinetics of CH 4 oxidation in oxic soils exposed to ambient air or high CH 4 mixing ratios. FEMS Microbiol Lett 1992; 101:261–270 [CrossRef]
    [Google Scholar]
  78. Hanson DT, Swanson S, Graham LE, Sharkey TD. Evolutionary significance of isoprene emission from mosses. Am J Bot 1999; 86:634–639 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  79. Zuo Z. Why algae release volatile organic compounds—the emission and roles. Front Microbiol 2019; 10:491 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  80. Srivastva N, Singh A, Bhardwaj Y, Dubey SK. Biotechnological potential for degradation of isoprene: a review. Crit Rev Biotechnol 2018; 38:587–599 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  81. Srivastva N, Singh RS, Upadhyay SN, Dubey SK. Degradation kinetics and metabolites in continuous biodegradation of isoprene. Bioresour Technol 2016; 206:275–278 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  82. Wagner M. Single-Cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Annu Rev Microbiol 2009; 63:411–429 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  83. Prior SD, Dalton H. Acetylene as a suicide substrate and active site probe for methane monooxygenase from Methylococcus capsulatus (Bath). FEMS Microbiol Lett 1985; 29:105–109 [CrossRef]
    [Google Scholar]
  84. Alvarez HM, Mayer F, Fabritius D, Steinbüchel A. Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch Microbiol 1996; 165:377–386 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  85. Crombie AT, Emery H, McGenity TJ, Murrell JC. Draft genome sequences of three terrestrial isoprene-degrading Rhodococcus strains. Genome Announc 2017; 5:e01256–01217 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  86. Boyd DR, Clarke D, Cleij MC, Hamilton JTG, Sheldrake GN. Bacterial biotransformation of isoprene and related dienes. Monatsh Chem 2000; 131:673–685 [CrossRef]
    [Google Scholar]
  87. Axcell BC, Geary PJ. Purification and some properties of a soluble benzene-oxidizing system from a strain of Pseudomonas. Biochem J 1975; 146:173–183 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  88. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [CrossRef][PubMed][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000931
Loading
/content/journal/micro/10.1099/mic.0.000931
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error